Abstract
Population fragmentation is often correlated with loss of genetic diversity and reduced fitness. Obligate out-crossing (dioecy) is expected to enhance genetic diversity, reduce genetic differentiation, and avoid inbreeding depression through frequent gene flow. However, in highly fragmented populations dioecy has only diminishing effects upon genetic structure as pollination limitations (e.g. flight distance of pollinators) most often restrict inter-population gene flow in insect pollinated species. In fragmented dry grasslands in northeastern Germany, we analysed genetic structure, fitness, and habitat quality of the endangered dioecious Silene otites (Caryophyllaceae). Using AFLP markers, a high level of differentiation among ten populations was found (F st = 0.36), while the intra-population genetic diversities (H E = 0.165–0.240) were similar as compared to hermaphroditic species. There was neither a correlation between geographic and genetic distance nor between genetic diversity and population size, which indicates reduced gene flow among populations and random genetic drift. Plant size was positively correlated with genetic diversity. Seed set and number of juveniles were positively related to population size. Higher total coverage resulted in reduced plant fitness, and the number of juveniles was negatively correlated to cryptogam cover. Additionally, we found a sex ratio bias towards more male plants in larger populations. Overall, our results indicate that on a regional geographic scale dioecy does not necessarily prevent genetic erosion in the case of habitat fragmentation, especially in the absence of long distance seed and pollen dispersal capacity.
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References
Barrett SCH (2010) Understanding plant reproductive diversity. Philos Trans R Soc Lond Ser B 365:99–109
Barrett SCH, Yakimowski SB, Field DL, Pickup M (2010) Ecological genetics of sex ratios in plant populations. Philos Trans R Soc Lond Ser B 365:2549–2557
Bates D, Maechler M, Dai B (2008) The lme4 Package. Available at: http://lme4.r-forge.r-project.org/ Accessed 10 June 2009
Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P (2004) How to track and assess genotyping errors in population genetics studies. Mol Ecol 13:3261–3273
Booy G, Hendriks RJJ, Smulders MJM, Van Groenendael JM, Vosman B (2000) Genetic diversity and the survival of populations. Plant Biol 2:379–391
Brantjes NBM, Leemans JAAM (1976) Silene otites (Caryophyllaceae) pollinated by nocturnal Lepidoptera and mosquitoes. Acta Bot Neerl 25:281–295
Campbell D, Duchesne P, Bernatchez L (2003) AFLP utility for population assignment studies: analytical investigation and empirical comparison with microsatellites. Mol Ecol 12:1979–1991
Cardé RT (2008) Animal migration: seasonal reversals of migrant moths. Curr Biol 18:1007–1009
Caruso CM, Case AL (2007) Sex ratio variation in gynodioecious Lobelia siphilitica: effects of population size and geographic location. J Evol Biol 20:1396–1405
Case AL, Ashman TL (2007) An experimental test of the effects of resources and sex ratio on maternal fitness and phenotypic selection in gynodioecious Fragaria virginiana. Evolution 61:1900–1911
Charlesworth D, Charlesworth B (1990) Inbreeding depression with heterozygote advantage and its effect on selection for modifiers changing the outcrossing rate. Evol 44:870–888
Crawley M (2007) The R Book. John Wiley, Chichester
Duffy KJ, Scopece G, Cozzolino S, Fay MF, Smith RJ, Stout JC (2009) Ecology and genetic of the dense-flowered orchid, Neotinea maculata, at the centre and edge of its range. Ann Bot 104:507–516
Duminil J, Hardy OJ, Petit RJ (2009) Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evol Biol 9:177
Ehrich D (2006) AFLPdat: a collection of R functions for convenient handling of AFLP data. Mol Ecol Notes 6:603–604
Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Ann Rev Ecol Sys 24:217–242
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Excoffier LGL, Schneider S (2006) Arlequin ver. 3.1: an integrated software package for population genetics data analysis. Computational and molecular population genetics lab (CMPG), University of Berne, Swizerland. Accessed 10 June 2008
Fischer M, Matthies D (1998) Effects of population size on performance in the rare plant Gentianella germanica. J Ecol 86:195–204
Freeman DC, Klikoff LG, Harper KT (1976) Differential resource utilization by the sexes of dioecious plants. Science 193:597–599
Giles BE, Goudet J (1997) Genetic differentiation in Silene dioica metapopulations: estimation of spatiotemporal effects in a successional plant species. Am Nat 149:507–526
Glemin S, Bazin E, Charlesworth D (2006) Impact of mating systems on patterns of sequence polymorphism in flowering plants. Proc R Soc B Biol Sci 273:3011–3019
Guibert C, Civeyrel L, Linder P (2009) Male and female separation event trapped in a species tree. Taxon 58:172–180
Hamrick JL, Godt MJW (1996) Effects of life history traits on genetic diversity in plant species. Philos Trans R Soc Lond Ser B Biol Sci 351:1291–1298
Hensen I, Oberprieler C (2005) Effects of population size on genetics diversity and seed production in the rare Dictamnus albus (Rutaceae) in Central Germany. Cons Gen 6:63–73
Hensen I, Oberprieler C, Wesche K (2005) Genetic structure, population size, and seed production of Pulsatilla vulgaris Mill. (Ranunculaceae) in Central Germany. Flora 200:3–14
Hensen I, Kilian C, Wagner V, Durka W, Pusch J, Wesche K (2010) Low genetic variability and strong differentiation among isolated populations of the rare steppe grass Stipa capillata L. in Central Europe. Plant Biol 12:526–536
Hilfiker K, Holderegger R, Rotach P, Gugerli F (2004) Dynamics of genetic variation in Taxus baccata: local versus regional perspectives. Can J Bot 82:219–227
Honnay O, Jacquemyn H (2007) Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Cons Biol 21:823–831
Honnay O, Adriaens D, Coart E, Jacquemyn H, Roldan-Ruiz I (2007) Genetic diversity within and between remnant populations of the endangered calcareous grassland plant Globularia bisnagarica L. Cons Genet 8:293–303
Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evol 50:54–70
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806
Jennersten O, Nilsson SG (1993) Insect flower visitation frequency and seed production in relation to patch size of Viscaria vulgaris (Caryophyllaceae). Oikos 68:283–292
Jhumur US, Dötterl S, Jürgens A (2008) Floral odors of Silene otites: their variability and attractiveness to mosquitoes. J Chem Ecol 34:14–25
Kalliovirta M, Ryttari T, Heikkinen RK (2006) Population structure of a threatened plant, Pulsatilla patens, in boreal forests: modelling relationships to overgrowth and site closure. Biodiv Cons 15:3095–3108
Korneck D, Schnittler M, Vollmer I (1996) Rote Liste der Farn- und Blütenpflanzen (Pteridophyta et Spermatophyta) Deutschlands. Schriftenreihe für Vegetationskunde 28:21–187
Kwak MM, Velterop O, van Andel J (1998) Pollen and gene flow in fragmented habitats. Appl Veg Sci 1:37–54
Langhans TM, Storm C, Schwabe A (2009) Biological soil crusts and their microenvironment: Impact on emergence, survival and establishment of seedlings. Flora 204:157–168
Lauterbach D, Burkart M, Gemeinholzer B (accepted) Rapid genetic differentiation between ex situ and their in situ source populations: an example of the endangered Silene otites (Caryophyllaceae). Bot J Linn Soc
Lauterbach D, Ristow M, Gemeinholzer B (2011) Genetic population structure, fitness variation and the importance of population history in remnant populations of the endangered plant Silene chlorantha (Willd.) Ehrh. (Caryophyllaceae). Plant Biol 13:667–777
Leimu R (2010) Habitat quality and population size as determinants of performance of two endangered hemiparasites. Ann Bot Fennici 47:1–13
Leimu R, Mutikainen P (2005) Population history, mating system, and fitness variation in a perennial herb with a fragmented distribution. Cons Biol 19:349–356
Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation? J Ecol 94:942–952
Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. Ann Rev Ecol Sys 27:237–277
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Ann Rev Ecol Sys 15:65–95
Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99
Maurer K, Weyand A, Fischer M, Stöcklin J (2006) Old cultural traditions, in addition to land use and topography, are shaping plant diversity of grasslands in the Alps. Biol Conserv 130:438–446
Moyle LC (2006) Correlates of genetic differentiation and isolation by distance in 17 congeneric Silene species. Mol Ecol 15:1067–1081
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nilsson E, Agren J (2006) Population size, female fecundity, and sex ratio variation in gynodioecious Plantago maritima. J Evol Biol 19:825–833
Obbard DJ, Harris SA, Pannell JR (2006) Sexual systems and population genetic structure in an annual plant: testing the metapopulation model. Am Nat 167:354–366
Paschke M, Abs C, Schmid B (2002) Relationship between population size, allozyme variation, and plant performance in a narrow endemic Cochlearia bavarcia. Cons Gen 3:131–144
Peterson A, Bartish IV, Peterson J (2008) Effects of population size on genetic diversity, fitness and pollinator community composition in fragmented populations of Anthericum liliago L. Plant Ecol 198:101–110
Pless H (1994) Pflanzensoziologische Untersuchungen der Trockenrasen an den Hängen des Odertales im Kreis Seelow (Brandenburg). Diplomarbeit, Göttingen
Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes consequences, and solutions. Nat Rev Genet 6:847–859
Poschlod P, WallisDeVries MF (2002) The historical and socioeconomic perspective of calcareous grasslands–lessons from the distant and recent past. Biol Cons 104:361–376
Poschlod P, Bakker JP, Kahmen S (2005) Changing land use and its impact on biodiversity. Basic Appl Ecol 6:93–98
Prasse R, Ristow M, Klemm G, Machatzi B, Raus T, Scholz H, Stohr G, Sukopp H, Zimmermann F (2001) Liste der wildwachsenden Gefäßpflanzen des Landes Berlin—mit Roter Liste. Kulturbuch-Verlag, Berlin
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rambaut A (2008) FigTree v1.2. Available at http://tree.bio.ed.ac.uk/software/FigTree/. Accessed 10 June 2009
R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org. Accessed June 2008
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Cons Biol 17:230–237
Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606
Richards CN, Emery SN, McCauley DE (2003) Genetic and demographic dynamics of small populations of Silene latifolia. Heredity 90:181–186
Ristow M, Herrmann A, Illig H, Klemm G, Kummer V, Kläge HC, Machatzi B, Rätzel S, Schwarz R, Zimmermann F (2006) Liste und Rote Liste der etablierten Gefäßpflanzen Brandenburgs. Naturschutz und Landschaftspflege in Brandenburg 15(4):1–163
Ronikier M (2002) The use of AFLP markers in conservation genetics—a case study on Pulsatilla vernalis in the polish lowlands. Cell Mol Biol Lett 7:677–684
Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Schmidt K, Jensen K (2000) Genetic structure and AFLP variation of remnant populations in the rare plant Pedicularis palustris (Scrophulariaceae) and its relation to population size and reproductive components. Am J Bot 87:678–689
Schulz A (1905) Das Blühen von Silene otites. Beihefte zum Botanischen Zentralblatt 18:433–446
Singh M, Chabane K, Valkoun J, Blake T (2006) Optimum sample size for estimating gene diversity in wild wheat using AFLP markers. Genet Resour Crop Evol 53:23–33
Soldaat LL, Vetter B, Klotz S (1997) Sex ratio in populations of Silene otites in relation to vegetation cover, population size and fungal infection. J Veget Sci 8:697–702
Soldaat LL, Lorenz H, Trefflich A (2000) The effect of drought stress on the sex ratio variation of Silene otites. Folia Geobotanica 35:203–210
Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440
Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland
Tero N, Aspi J, Siikamäki P, Jäkäläniemi A, Tuomi J (2003) Genetic structure and gene flow in a metapopulation of an endangered plant species, Silene tatarica. Mol Ecol 12:2073–2085
Tsuda Y, Komagata O, Kasai S, Hayashi T, Nihei N, Saito K, Mizutani M, Kunida M, Yoshida M, Kobayashi M (2008) A mark-release-recapture study on dispersal and flight distance of Culex pipiens pallens in an urban area of Japan. J Am Mosq Control Assoc 24:339–343
Tutin TG, Burges NA, Chater AO, Edmondson JR, Heywood VH, Moore DM, Valentine DH, Walters SM, Webb DA (1993) Flora Europaea Vol. 1. Psilotaceae to Platanaceae, second ed. Cambridge University Press, Cambridge
Ueno N, Suyama Y, Seiwa K (2007) What makes the sex ratio female-biased in the dioecious tree Salix sachalinensis? J Ecol 95:951–959
Vandepitte K, Honnay O, De Meyer T, Jacquemyn H, Roldan-Ruiz I (2010) Patterns of sex ratio variation and genetic diversity in the dioecious forest perennial Mercurialis perennis. Plant Ecol 206:105–114
Vekemans X (2002) AFLP-SURV version 1.0. Laboratoire de Génétique et Ecologie Végétale, Université Libre de Bruxelles, Belgium
Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Springer, New York
Vos P, Hogers R, Bleeker M, Reijans M, van de Lee T, Hornes M, Frijters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Watt AS (1981) A comparison of grazed and ungrazed grassland a in East Anglian breckland. J Ecol 69:499–508
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol 38:1358–1370
Wessels-de Wit S, Schwabe A (2010) The fate of sheep-dispersed seeds: Plant species emergence and spatial patterns. Flora 205:56–665
Wilson WG, Harder LD (2003) Reproductive uncertainty and the relative competiveness of simultaneous hermaphroditism versus dioecy. Am Nat 162:220–241
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. TREE 11:413–418
Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8:907–913
Zhou HP, Chen J (2010) Spatial genetic structure in an understorey dioecious fig species: the roles of seed rain, seed and pollen-mediated gene flow, and local selection. J Ecol 98:1168–1177
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This work was funded by the DBU and Heidehofstiftung. We would like to thank the local nature conservation authorities for the collection permission in conservation areas and Hans Pfestorf for help in the field.
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Lauterbach, D., Ristow, M. & Gemeinholzer, B. Population genetics and fitness in fragmented populations of the dioecious and endangered Silene otites (Caryophyllaceae). Plant Syst Evol 298, 155–164 (2012). https://doi.org/10.1007/s00606-011-0533-0
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DOI: https://doi.org/10.1007/s00606-011-0533-0